Involvement of the Meto/Msr System in Two Acer Species That Display Contrasting Characteristics During Germination

International Journal of Molecular Sciences Article Involvement of the MetO/Msr System in Two Acer Species That Display Contrasting Characteristics during Germination Natalia Wojciechowska 1,2 , Shirin Alipour 1 , Ewelina Stolarska 1, Karolina Bilska 1, Pascal Rey 3 and Ewa M. Kalemba 1,* 1 Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland; [email protected] (N.W.); [email protected] (S.A.); [email protected] (E.S.); [email protected] (K.B.) 2 Department of General Botany, Institute of Experimental Biology, Faculty of Biology, Adam Mickiewicz University, Uniwersytetu Poznańskiego6, 61-614 Poznań,Poland 3 Plant Protective Proteins (PPV) Team, Centre National de la Recherche Scientifique (CNRS), Commissariat à l’Energie Atomique et aux Energies Alternatives (CEA), Biosciences and Biotechnology Institute of Aix-Marseille (BIAM), Aix Marseille University (AMU), 13108 Saint Paul-Lez-Durance, France; [email protected] * Correspondence: [email protected]; Tel.: +48-61-8170033 Received: 7 October 2020; Accepted: 1 December 2020; Published: 2 December 2020 Abstract: The levels of methionine sulfoxide (MetO) and the abundances of methionine sulfoxide reductases (Msrs) were reported as important for the desiccation tolerance of Acer seeds. To determine whether the MetO/Msrs system is related to reactive oxygen species (ROS) and involved in the regulation of germination in orthodox and recalcitrant seeds, Norway maple and sycamore were investigated. Changes in water content, MetO content, the abundance of MsrB1 and MsrB2 in relation to ROS content and the activity of reductases depending on nicotinamide adenine dinucleotides were monitored. Acer seeds differed in germination speed—substantially higher in sycamore—hydration dynamics, levels of hydrogen peroxide, superoxide anion radicals (O ) and hydroxyl radicals ( OH), 2•− • which exhibited peaks at different stages of germination. The MetO level dynamically changed, particularly in sycamore embryonic axes, where it was positively correlated with the levels of O2•− and the abundance of MsrB1 and negatively with the levels of OH and the abundance of MsrB2. • The MsrB2 abundance increased upon sycamore germination; in contrast, it markedly decreased in Norway maple. We propose that the ROS–MetO–Msr redox system, allowing balanced Met redox homeostasis, participates in the germination process in sycamore, which is characterized by a much higher speed compared to Norway maple. Keywords: methionine oxidation; nicotinamide adenine dinucleotide phosphate; redox posttranslational modification; reactive oxygen species; methionine sulfoxide reductase; seeds 1. Introduction Seeds are evolutionarily important structures enabling plant reproduction. Seed germination and successful seedling establishment allow the installation of the next generation of plants. Seed germination is a complex physiological trait that can be prevented or delayed by dormancy [1–3]. The model of seed germination consists of three phases: seed imbibition, which is manifested by water uptake (first phase), re-initiation of metabolic processes (second phase) and postgermination growth (third phase), which refers to a further increase in water uptake that results in embryo expansion [1]. Germination sensu stricto involves first and second phases [1–3]. The molecular basis of the changes Int. J. Mol. Sci. 2020, 21, 9197; doi:10.3390/ijms21239197 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 9197 2 of 21 in morphology, structure, metabolism, hormones and gene expression during seed germination is well characterized in Arabidopsis [4,5]. Among phytohormones, abscisic acid (ABA), giberrellins (GAs) and ethylene (ET) primarily regulate seed dormancy and germination in dicot species [6,7], notably through interplay with reactive oxygen species (ROS) [8,9]. Many studies confirmed that hormonal regulation of germination has effects at the transcriptional and proteome levels [10,11] and eventually results in global changes in enzyme activity [12]. Global interactions exist also at the transcriptome level in germinating seeds [13]. Dry mature seeds can accumulate over 10,000 mRNAs intended for the synthesis of proteins associated with redox regulation, glycolysis and protein metabolism [14]. Importantly, the activity of many enzymes is redox-regulated [12], and their oxidized forms in mature dry seeds are reduced during imbibition for metabolism restoration [15]. In this context, redox posttranslational control of seed germination has emerged as an extremely important process [14,16]. ROS are assumed to be signaling molecules, and the interplay between ROS-related transduction pathways and others, such as hormone-related pathways, is well described [17–21]. Among ROS, the signaling role of hydrogen peroxide (H2O2) is widely studied, particularly in plant acclimation to stress and during growth and development [22–24]. ROS are signaling molecules in seeds that modulate dormancy disruption and germination [25,26] and are involved in endosperm deterioration and seed reserve mobilization [27]. Three ROS, H2O2, superoxide anion radicals (O2•−) and hydroxyl radicals ( OH), have been implicated in germination, particularly in root development [28–30]. H O and • 2 2 O2•− were demonstrated to be associated with cell differentiation and proliferation, respectively [30]. Postgerminative axis growth involves O2•− production [31–33]. Less attention has been paid to the role of the short-lived but most reactive ROS, OH [34]. Indeed, OH is involved in germination [35–37]. • • More and more evidences indicate that OH could be targeted to play a role in plant cell wall loosening • thus placing these reactive molecules as important components involved in plenty of developmental processes [38]. Miller [39] and Fry [38] showed that cell-wall polysaccharides such as pectin and xyloglucan can be broken down by OH. Further analyses confirmed that OH production in the • • apoplast causes scission of specific cell wall polysaccharides in elongating maize coleoptiles as well as in the radicles and endosperm caps of germinating cress seeds [35]. ROS are thus signaling molecules involved in the regulation of seed germination [25]. Nucleic acids, especially RNA, and proteins are the most sensitive molecules to oxidation [40]. Targeted mRNA oxidation can fine-tune the cell signaling pathway that controls germination via selective translation [41]. Massive protein oxidation occurs during germination [42,43]. Importantly, selective oxidation of both mRNA and proteins is necessary for completing germination [25,27,41,44]. ROS damage to proteins can be irreversible and irreparable (i.e., carbonylation) [45]. Reversible protein oxidative modifications involve cysteine (Cys) and methionine (Met), which are the two amino acids the most prone to oxidation by ROS [46]. Oxidation of Met to methionine sulfoxide (MetO) is reversed via the action of enzymes termed methionine sulfoxide reductases (Msrs), including several isoforms that are classified as one of two types, A and B [36,37,47–51]. The Met-MetO-Met transition in proteins is considered a redox switch-regulating activity [48] in relation to ROS-initiated signaling. The reversibility of the Met redox status depends on the activity of the Msrs system, which in turn depends on the presence of redoxins and reducing agents that can regenerate Msrs [37,52]. Met metabolism was demonstrated to be essential to seed germination [16]. More precisely, proteins associated with Met synthesis and the recycling pathway [10] were identified as important for dormancy disruption [53]. However, Met redox homeostasis has never been investigated in this context. Norway maple (Acer platanoides L.) and sycamore (Acer pseudoplatanus L.) belong to the same genus but produce desiccation-tolerant and desiccation-sensitive seeds, respectively. The comparison of Norway maple and sycamore seeds became a model for studying differences between orthodox and recalcitrant seeds at important transitions, such as development [54,55], dormancy acquisition [53,56] and drying/desiccation [57–61]. However, the germination process was studied uniquely in the two species in the context of nuclear replication activity [62] and hormonal regulation [11]. Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 3 of 21 uniquely in the two species in the context of nuclear replication activity [62] and hormonal regulation [11]. Int. J. Mol.The Sci. seeds2020 ,of21 ,these 9197 two contrasting Acer species were characterized by distinct levels of 3ROS, of 21 MetO, MsrB1 and MsrB2 and differences in the activity of NADPH‐dependent reductases during the developmentThe seeds and of thesematuration two contrasting phases [63]Acer as wellspecies as during were characterized dehydration byand distinct desiccation levels [64]. of ROS, The MetO,MetO/Msr MsrB1 system and MsrB2was assumed and diff erencesto be involved in the activity in the ofestablishment NADPH-dependent of desiccation reductases tolerance during in theorthodox development Norway and maple maturation seeds [64]. phases Thus, [63 it] was as well necessary as during to determine dehydration whether and desiccation the MetO/Msr [64]. Thesystem MetO participates/Msr system in wasthe regulation assumed to of be germination, involved in theduring establishment which Norway of desiccation maple and tolerance sycamore in orthodoxseeds cease Norway to be mapledifferent seeds in [terms64]. Thus, of desiccation it was necessary tolerance to determine

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